Physiological and molecular mechanisms of cold deacclimation for timely balancing stress release with growth resumption

In autumn, temperate plants cold acclimate, whereby they become increasingly freezing tolerant. Maximum freezing tolerance is reached midwinter, and upon exposure to warmer temperatures in spring plants lose acclimated freezing tolerance by the process of deacclimation. The timing and rate of deacclimation are key determinants of the risk of late-winter and spring frost damage to perennial crops and associated reductions in fruit yield, plant quality or survival. Paradoxically, as the climate warms, the risk of late-frost damage to plants is forecasted to increase in many regions of the world. While cold acclimation has been investigated in detail, relatively little is known about which traits make plants vulnerable to frost damage in late winter and spring and the physiological, metabolic and molecular mechanisms of deacclimation. Most extensively documented is decreasing contents of sugars and amino acids and increasing starch content, indicating diversion of resources from maintenance of freezing tolerance to fuel for growth resumption. Deacclimation is also characterized by saturation of membrane lipids and a distinct decrease in the abundance of stress- or defense-related proteins, and an increase of proteins related to renewed growth. The molecular mechanisms of deacclimation in woody perennials are not well understood, but according to data from herbaceous plants, hormonal regulation appears particularly important during deacclimation, with extensive changes in the expression of genes related to hormone metabolism and induction of transcription factor families that control fundamental aspects of morphogenesis and development. Collectively, deacclimation involves two inter-related processes that result in a reduction of freezing tolerance and a reinitiation of growth and development. In this paper, recent advances in our understanding of deacclimation mechanisms in mostly woody horticultural perennials are reviewed and possible future research directions are highlighted.